Incidence and biomarkers of pregnancy, spontaneous abortion, and neonatal loss during an environmental stressor: Implications for female reproductive suppression in the cooperatively breeding meerkat

Abstract

Meerkats are group-living, insectivorous herpestids in which subordinate members provide extensive care for the dominant female's young. In contrast to some cooperative breeders, subordinate female meerkats are physiologically able to reproduce and occasionally do so successfully; their attempts are more frequently 'suppressed' via eviction or infanticide by the dominant female. Spontaneous abortion and neonatal loss occur with some regularity, further negatively impacting reproductive success. Here, we compared the reproductive outcomes and endocrine profiles, including of serum progesterone (P), serum estradiol (E), and fecal glucocorticoid metabolites (fGCm), of dominant and subordinate dams residing within their clans in the Kalahari Desert of South Africa. Our study spanned years of drought, which reduced insect abundance and represented a substantial environmental stressor. Meerkat pregnancies were identified at mid-term and culminated either in spontaneous abortions or full-term deliveries, after which pups were either lost prior to emergence from the natal den (usually within 2days of birth) or emerged at 2-3weeks. Neonatal loss exceeded fetal loss for all females, and contributed to narrowing the status-related disparity in female reproductive output seen during less arid periods. Although E concentrations were significantly lower in subordinate than dominant females, they were sufficient to support gestation. Absolute E concentrations may owe to androgenic precursors that also attain highest concentrations in dominant dams and may mediate aggression underlying female reproductive skew. Pregnancies terminating in fetal loss were marked by significantly lower P concentrations in mid-gestation and modestly lower E concentrations overall. Consistently high fGCm concentrations further increased across trimesters, particularly (but not consistently) in subordinates and in aborted pregnancies. Environmental stressors may modulate reproductive outcomes in meerkats through their influence on sex steroids and their effects on intragroup competition. The social and eco-physiological factors affecting intraspecific variation in reproductive output, even in obligate cooperative breeders, may be most apparent during extreme conditions, reflecting the benefits of long-term studies for assessing the impact of climate change.

Steroids, Pregnancy and Fetal Development

“…across pregnancy (53), stressful stimuli can still elicit the secretion of glucocorticoids in mouse and humans (6,64). Concomitantly, stress challenges reduce progesterone levels during pregnancy in mammals (65)(66)(67)(68). This could result from impaired steroidogenesis in the ovary, e.g., due to poor stimulation by placental lactogens (68).…”

Social and endocrine correlates of immune function in meerkats: implications for the immunocompetence handicap hypothesis

“…Upon acquiring dominance, male and female meerkats experience energetic costs that could further limit their immune function: notably, males engage in energetically expensive bouts of scent marking and mate guarding [39], and females, beyond engaging in dominance assertions and aggressively targeting subordinate dams [72], are frequently pregnant [32,33,41,73]. Yet, consistent with immunocompetence in other species [74,75] and with parasitism in meerkats [23], we found no evidence that pregnancy, per se , was linked to immunosuppression.…”

“…In a species characterized by such extreme food competition [83], perhaps priority of access to large, non-monopolizable resources buffers dominant female hyaenas from immunological trade-offs [9]. By contrast, the small, monopolizable food resources of meerkats may minimize the impact of food competition [33] on their immune function. Moreover, in spotted hyaenas, rank in a linear dominance hierarchy is maternally acquired [83,84], whereas in meerkats, individuals compete for breeding status in a despotic society [32].…”

“…We classified males as roving if they had been absent from the group in the 2 days before or after sample collection [22]. We classified females as pregnant at the time of sampling based on weight gain and abdominal swelling [33]. …”

“…Again, among females, but not males, dominance is associated with greater concentrations of sex hormones (i.e. A 4 , T and oestradiol or E 2 ) [22,31–33]. A dominant female's raised hormone concentrations may be linked to increased aggressiveness, enabling her to control reproduction by thwarting potential rivals, forcibly evicting subordinate dams or killing their offspring [32,40,41].…”